Frontiers in Zoology BioMed Central

Review Open Access Biogeographical and evolutionary importance of the European high systems Thomas Schmitt

Address: Biogeographie, Fachbereich VI, Wissenschaftspark Trier-Petrisberg, Universität Trier, D – 54286 Trier, Germany Email: Thomas Schmitt - [email protected]

Published: 29 May 2009 Received: 11 February 2009 Accepted: 29 May 2009 Frontiers in Zoology 2009, 6:9 doi:10.1186/1742-9994-6-9 This article is available from: http://www.frontiersinzoology.com/content/6/1/9 © 2009 Schmitt; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Abstract is characterised by several high mountain systems dominating major parts of its area, and these structures have strongly influenced the evolution of taxa. For species now restricted to these high mountain systems, characteristic biogeographical patterns of differentiation exist. (i) Many local endemics are found in most of the European high mountain systems especially in the and the more geographically peripheral regions of Europe. Populations isolated in these peripheral mountain ranges often have strongly differentiated endemic genetic lineages, which survived and evolved in the vicinity of these mountain areas over long time periods. (ii) Populations of taxa with wide distributions in the Alps often have two or more genetic lineages, which in some cases even have the status of cryptic species. In many cases, these lineages are the results of several centres of glacial survival in the perialpine areas. Similar patterns also apply to the other geographically extended European high mountain systems, especially the Pyrenees and Carpathians. (iii) Populations from adjoining high mountain systems often show similar genetic lineages, a phenomenon best explained by postglacial retreat to these from one single differentiation centre between them. (iv) The populations of a number of species show gradients of genetic diversity from a genetically richer East to a poorer West. This might indicate better glacial survival conditions for this biogeographical group of species in the more eastern parts of Europe.

Background in their biogeography and evolution by the complexity of The evolution within species and sibling species com- the European high mountain systems. plexes in Europe is closely connected to the range shifts caused by the cyclic changes between relatively short and The Mediterranean species survived the cold stages of the warm, mostly humid and longer cold and predominantly Pleistocene in the Mediterranean Basin and expanded dry periods [1,2]. These climatic shifts resulted in large northwards during the postglacial [7,8]. These expansions scale range shifts in many species often resulting in dis- are largely shaped by the high mountain systems of the junct distribution pattern during at least one of these Alps and Pyrenees acting as dispersal barriers of different phases [3,4]. However, the effects of these climatic fluctu- strength so that four different paradigms of postglacial ations vary considerably in different ecological and distri- range expansions from the three Mediterranean peninsu- butional groups [5,6], and three major groups can be las can be distinguished [9,10]. In contrast to the assump- distinguished: Mediterranean, continental and / tions made by de Lattin [6], the continental species, which alpine species [2], which are all to some degree influenced in most cases have not immigrated into Europe from Asi-

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atic core areas during the postglacial, had so called extra- just one of them. As the Alps are by far the most extensive Mediterranean refuge and differentiation centres north of and highest mountain system of Europe, it is not surpris- the typical Mediterranean refugia. These were also ing that the highest number and amount of endemics of strongly influenced by the European mountain systems typical high mountain species is found in this mountain because they offered suitable refuge areas in their non-gla- range, as for example demonstrated by lepidopterans and ciated parts during ice ages and acted as dispersal barriers especially in the little mobile group of the micro-moths during postglacial range shifts [e.g. [11-19]]. [20]. Some of these alpine endemics (in as well as in plants) are widespread all over this mountain area, The group of alpine and arctic-alpine species is most stretching almost the entire range from Nice in the south- strongly shaped in their biogeographical and evolutionary west to Vienna in the northeast (in many cases showing history by the geographic location and complexity of the remarkable genetic substructure, see below); while others different European high mountain systems because (i) are more or less local endemics of some parts of the Alps. these species are now restricted to these mountain ranges and (in some cases) the arctic and (ii) most of their actual Two types of hotspots for local endemics of the Alps can distribution areas were covered by extensive ice-shields be distinguished: during the glacial periods [5,20]. In general, we can distin- guish between several different distributional types in (i) Species with their ranges restricted to peripheral these mountain species. Thus, Varga and Schmitt [20] dis- regions of the Alps and mostly confined to lower and tinguish between five major patterns: (i) endemics of the intermediate (e.g. observed in some Alps restricted to some parts or the entire range, (ii) the species, Lycaenids etc.; for details see Varga & Schmitt "Alpine archipelago" with the species' strongholds in the [20]). The largest concentrations of these local endem- Alps and other parts of the range in adjoining mountain ics are in the regions of the southwestern and the ranges, but without long distance disjunctions, (iii) southeastern Alps, two regions with larger areas at mountain species with long distance disjunctions in lower altitudes not covered by ice during glaciations. Europe (e.g. in the mountains of the Balkan Peninsula, These ice-free areas most probably served as centres of or Iberia), (iv) oro-Mediterranean species with their glacial survival, from where these species only per- ranges mostly restricted to the mountains of the summer- formed altitudinal shifts, but no major range expan- arid high mountain systems of southern Iberia, southern sions over large parts of the deglaciating Alps. As these Italy and the southern Balkan Peninsula and (v) arctic- taxa might have performed these altitudinal shifts alpine species with a disjunction between mountain pop- repeatedly through the climatic fluctuations of the ulations in the South (Alps, often also Pyrenees, Carpathi- Pleistocene, these refuge areas might also be the loca- ans, Balkan high mountain systems) and a large zonal tions of the evolutionary process of speciation [1]. range in the Arctic. However, genetic analyses in this group of species are scarce and in butterflies restricted to the three taxa However, the distribution histories and evolutionary Coenonympha darwiniana [30], C. macromma [30] and processes underlying these different distributional types Erebia sudetica inalpina (Figure 1) [31]. The latter is in mountain species are still poorly understood. There- today confined to the region of Grindelwald (Berner fore, I summarise the known examples and extract the Oberland, northwestern Alps) and most probably sur- repetitive pattern. Examples are preferably taken from the vived at least the last glaciation in a geographically butterflies because this group is well studied and suitable restricted refuge area northwest of the Alpine ice- for biogeographical analyses [e.g. [21-29]], but where nec- shield, likely suffering population bottlenecks and essary other groups and even plants are referenced. subsequent genetic erosion [31]. The two Coenonym- In this article, I especially focus on two questions: pha taxa are restricted to the south-central Alps (C. dar- winiana) and the Alpes Maritimes (C. macromma). (1) Which repetitive biogeographical and evolutionary Both might have survived also at least the last ice age patterns are characteristic for European mountain species? at lower elevations close to their recent distributions [30]. (2) What is the influence of the climatic cycles on their dif- ferentiation? (ii) Species restricted to some parts of the Inner Alps, as for example a number of (often flightless) micro- Endemics and endemic genetic lineages of high moth species [32] and beetles [5], but only a single mountain systems butterfly species (i.e. Erebia nivalis) [20]. These species Endemics of the Alps in general are confined to high alpine habitats and Most of the larger European high mountain systems pos- may have survived glaciations in situ at so called Nuna- sess endemic species (or at least subspecies) confined to taks (i.e. small ice-free areas topping over the ice-

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EuropeanFigureGeographicmtDNA 2 sequences mountain distribution ofsystems the of caddisfly twelve genetic Drusus lineagesdiscolor inbased the on Geographic distribution of twelve genetic lineages based on mtDNA sequences of the caddisfly Drusus allozymeGeographicterflyFigure species 1 polymorphisms distribution complex in of ofthe thr the Alpsee Erebia genetic melampus lineages/ sudeticabased on but- discolor in the European mountain systems. Each line- Geographic distribution of three genetic lineages age is presented in a different colour; separate areas marked based on allozyme polymorphisms of the Erebia by identical colour harbour the same lineage. Redrawn from melampus/sudetica butterfly species complex in the Pauls et al. [41]. Alps. (Red: western Alpine E. melampus; blue: eastern Alpine E. melampus; green: E. sudetica inalpina). Redrawn from Hau- brich & Schmitt [31]. lineages of the beetle Nebria rufescens and the butterfly Ere- bia pandrose, two arctic-alpine species, were found here shield of the Inner Alps). For animals, survival in these [42]; a strongly differentiated genetic lineage was also areas is only supported by chorological data sets (i.e. found in the Proclossiana eunomia populations from the distribution pattern) [5,20], but genetic data in plants Stara Planina [39]. In the spiders of the Pardosa saltuaria give some support for these refuges (see Schönswetter species group, the populations from the Bulgarian moun- et al. [33] for a recent review, [34,35]). tains, and also from the Pyrenees, showed a strong differ- entiation from a northern clade including the Alps, Endemics of other high mountain systems of Europe Carpathians, some middle high mountains of Central Although the Alps are the European mountain system Europe and Scandinavia (Figure 3) [43]. The caddisfly with the highest number of endemic species, numerous Drusus discolor also showed strongly differentiated genetic endemic genetic lineages or taxa are known for almost all lineages for all of the marginal mountain systems of high mountain systems in parts of Europe not entirely Europe where the taxon occurs, including the high moun- being covered by ice during the glacial periods. However, tain systems of (Figure 2) [41]. Also plants in the there are peculiar differences between the more marginal Balkan high mountain systems showed strongly differen- (e.g. Cantabrian Mts., Bulgarian Mts.) and more central tiated genetic lineages from other regions of Europe [44]. (e.g. Carpathians, Massif Central, Apennines) mountain systems. Furthermore, the distribution pattern of some species and subspecies strongly support these observed genetic struc- Thus, the more marginal mountain areas of Europe have tures. Thus, the eastern Balkan mountains are the only particularly high proportions of old evolutionary units mountain range of the southern part of Europe where the (often with relict status) when compared to more geo- fairly widespread mountain ringlet Erebia epiphron is lack- graphically central mountain ranges. For example, cases of ing, but the species is substituted by its sister taxon Erebia such old genetic lineages are known for the flora of the orientalis supporting the strong evolutionary independ- Cantabrian Mts. in northwestern Spain [e.g. [36-38]]; the ence of this region. Regarding this latter species, each of number of examples in animals is rather low, but the the three mountain ranges harbouring it (i.e. , Pirin, known cases support the patterns observed in plants well, Stara Planina) has its own subspecies with strong mor- e.g. the butterfly Proclossiana eunomia [39,40] and the cad- phological differentiations among them [45,46]. A similar disfly Drusus discolor (Figure 2) [41]. situation is also observed for the only occurrences of Euphydryas cynthia outside the Alps: the male individuals Another stronghold of strongly differentiated genetic lin- of the Pirin population consistently have a considerably eages and endemic species is situated in the Bulgarian more extended white wing colouration than average pop- high mountain systems. Thus, the most distinct genetic ulations from the Alps, while the white colouration is

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strongly reduced in the Rila individuals [45]. This also below), but also have numerous endemic species (e.g. in underlines the evolutionary independence among these lepidopterans Erebia gorgone, three Sattleria species) mountain ranges of the eastern Balkan Peninsula on a [20,49]; their number however is much lower than in the fairly small geographic scale of sometimes only few tens Alps, which are considerably higher and much more of kilometres. extended. Many mountain species with larger distribu- tions show endemic lineages in the Pyrenees or parts of Such old lineages are fewer in the mountain systems with them, thereby supporting the idea of differentiation cen- closer geographic connections with the Alps (e.g. Car- tres at the lower elevations of the Pyrenean area and recent pathians, Massif Central), and genetic differentiations of (mostly postglacial) range shifts to higher altitudes of the these mountain systems from the Alps are often low; most mountains, as demonstrated for the butterflies Erebia epi- examples come from plants [e.g. [36,38,47,48]], but also phron (Figure 4) [50], Erebia euryale (Figure 5) [51], Erebia include the Pardosa saltuaria spider species group (Figure pandrose [42] and Erebia manto (unpublished data), but 3) [43]. On the species level, these mountain ranges also other animal [41,43] and plant species [36]. mostly share their species with the Alps. However, well distinguished subspecies are known for these mountain The summer-arid high mountain areas of the extreme species with many examples in the genus Erebia (e.g. E. south of Europe (especially southern Iberia and the south- epiphron, E. euryale, E. gorge, E. manto, E. melas) [49], but ern Balkan Peninsula) and the Maghreb (here in particu- the ages of these splits are mostly unknown and some lar the Atlas Mts.) do not have the typical alpine zonation even might be rather recent, even postglacial. [52], but show typical oro-Mediterranean characteristics. Some mountain species show local endemism to strongly The Pyrenees have an intermediate position, in which confined mountain blocks in this area as e.g. known for a they show some close connections to the Alps (see number of butterfly species [20,45,49]. These species in many cases represent relicts of often old invasions of spe- cies with their closed biogeographical connections to Cen- tral Asia [20,53,54].

Different genetic lineages within one high mountain system The large high mountain systems of the southern part of Europe (i.e. Pyrenees, Alps and Carpathians) have in many cases been colonised after the postglacial deglacia- tion by several genetic lineages, which have survived at least the last glacial period in several allopatric refugial areas often adjoining these high mountain systems.

Different genetic lineages in the Alps The Alps as the largest European high mountain system show a remarkable phylogeographic structure in many species. In plants, a differentiation into four genetic units along the Alps seems the most common feature with these lineages typically being confined to the southwestern, western central, eastern central and eastern Alps and the eastern lineages more often being of higher genetic diver- sity than the more western ones [2,33,42]. A quite similar pattern to that in many plant species was proposed for the leaf beetle Oreina elongata [55]. Also other animals fre- quently show different genetic lineages in the Alps, but saltuariaFiguremtDNAGeographic 3insequences the distribution European of the of mountain spider three speciesgenetic systems complexlineages and Scandinavia based Pardosa on their number is often less than in plants, and in many Geographic distribution of three genetic lineages based on mtDNA sequences of the spider species cases, only a western and an eastern lineage can be distin- complex Pardosa saltuaria in the European mountain guished. This is the case in the two butterflies Erebia mela- systems and Scandinavia. Each lineage is presented in a mpus (Figure 1) [31] and Erebia euryale (Figure 5) [51], the different colour; separate areas marked by identical colour wolf spiders species group Pardosa saltuaria (Figure 3) [43] harbour the same lineage. Redrawn from Muster & Beren- and the caddisfly Drusus discolor (Figure 2) [41]. In the first donk [43]. case, two strongly differentiated lineages (supported by allozyme polymorphisms [31] and differences in the male

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genitalia [56]) can be distinguished with a contact zone running north-south through Tyrol and along the Adige/ Etsch valley (maybe with some hybridisation in a limited area of southeastern and South Tyrol). The differentiation between these two lineages is rather advanced, and they most probably represent different spe- cies, with the eastern lineage showing a significantly higher genetic diversity than the western one [31]. These genetic and morphological differences are best explained by allopatric differentiation in two centres; and as the beginning of the first split is assumed to be older than the last ice age, the location of the initial differentiation cen- tres must remain enigmatic. However, the most likely Würm glacial refuge centres are in the hilly areas south of the Upper Italian Lakes for the western lineage and in the lower areas of the southeastern Alps (eastern Carinthia, Styria, Friul, parts of Slovenia) for the eastern theFigureGeographicallozyme western 4 polymorphisms distributionEuropean mountain of of five the genetic butterfly systems lineages Erebia basedepiphron on in lineage. Based on the higher genetic diversities of the pop- Geographic distribution of five genetic lineages based ulations belonging to the eastern lineage, we may assume on allozyme polymorphisms of the butterfly Erebia that the survival conditions were more suitable in this epiphron in the western European mountain systems. Each lineage is presented in a different colour; separate areas eastern region and/or this refuge area was geographically marked by identical colour harbour the same lineage and are considerably more extended than the more western refuge linked by a dotted line in the same colour. Redrawn from [31]. A very similar pattern was observed for Erebia euryale Schmitt et al. [50]. (Figure 5) with the only difference that survival of the western lineage is more likely around the southwestern Alps [51]. The caddisfly Drusus discolor repeats this geo- include populations from more than one part of the Car- graphic structure of a western and an eastern Alpine line- pathian arc. However, compiling existing data for differ- age (Figure 2) [41]. A much more complicated case is ent plant species revealed a generally lower genetic known in the butterfly Erebia epiphron [50]. This species diversity of the populations in the Carpathians than in the comprises four strongly differentiated lineages in the Alps: Alps, maybe due to higher topographic isolation of alpine western Alps, Aosta valley, northern Alps and eastern Alps habitats in the Carpathians [58]. (Figure 4). These lineages most probably evolved in four differentiation centres west, south, southeast and north of One study on animals that included a considerable the Alps, often linking the Alps with other mountain sys- number of samples from the Carpathian region was per- tems (see below). formed on the caddisfly Drusus discolor and showed a remarkable differentiation between the northwestern and Different genetic lineages in the Pyrenees the southern Carpathians (Figure 2). This thus supports As in the Alps, more than one genetic lineage per species the idea of a long lasting separation between these two is also observed in mountain elements of the Pyrenees parts of this high mountain system predating at least the [20]. However, the Pyrenees are considerably less last glaciation [41]. Similar cases are also reported for extended than the Alps, and the maximum number of dif- plants as Hypochaeris uniflora [59] and Campanula alpina ferent lineages found here is not as high as in the Alps; [60]. many species do not show marked differentiation over the Pyrenees. As an example, two different lineages are Thus, multiple glacial survival centres exist along the Car- observed in the Pyrenees for Erebia epiphron (Figure 4), pathian arc, as in the cases of the Pyrenees and especially one in the western and the other in the eastern parts of Alps, but the number of known cases is still rather limited. these mountains, with the first one most probably surviv- Therefore, a research focus on the phylogeography of the ing the last ice age north and the second in the southeast- Carpathians is needed. ern parts of the Pyrenees [50]. Also for the plant Cardamine alpina, AFLP patterns suggest survival in multi- Genetic links between different high mountain ple Pyrenean refugia [57]. systems As many of the glacial differentiation centres were not Different genetic lineages in the Carpathians restricted to the foot- of the respective high mountain Although being the largest high mountain system of east- systems, but were located in the (hilly) areas between high ern/southeastern Europe, only a few genetic analyses mountain systems, many links (by species and genetic lin-

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eages) can be observed between adjoining high mountain Nevertheless, many examples also revealed long-lasting systems, especially between (i) Pyrenees and southwest- separations between the populations from the Alps and ern Alps, (ii) northeastern Alps and northwestern Car- the Carpathians [57,60,65,70]. pathians, (iii) southeastern Alps and western Balkan mountains and (iv) southern Carpathians and the eastern Links between southeastern Alps and western Balkan Balkan high mountain systems [20]. In the following, mountains these connections are discussed using examples. The southeastern edge of the Alps is biogeographically strongly linked with the mountains of the western Balkan Links between Pyrenees and southwestern Alps Peninsula, as demonstrated by many occurrences of iden- The biogeographical links between the Pyrenees and the tical mountain beetle species in the southeastern Alps and Alps are seen in the occurrences of many taxa with the northwestern Balkan mountains [5,20]. While less in restricted distributions in these two areas, e.g. in lepidop- number, this distribution type is also known in the Lepi- terans by taxa as Euchloe simplonia, Polyommatus g. glandon, doptera for taxa like Coenonympha gardetta, Erebia otto- Aricia n. nicias, Erebia o. oeme [49]. However, the same mana, E. stirius, E. oeme spodia, E. epiphron aetheria and E. genetic lineages are also repeatedly found in these two styx trentae [49]. These distribution patterns support the regions, as in the case of Erebia cassioides [61] and Erebia survival of mountain species in the southeastern parts of epiphron (Figure 4), which has genetically very similar the Alps and adjoining areas (as demonstrated for Erebia populations in the western Pyrenees and the southwestern melampus (Figure 1) [31] and Erebia euryale (Figure 5) Alps, e.g. the Wallis in Switzerland [50]. The genetic simi- [51]), with postglacial retreat into the Alps in the north- larity in this case is best explained by a Würm glacial link west and the northwestern Balkan mountains in the between the Pyrenees and the Alps, and thus a more wide- southeast. spread distribution in the hilly regions of between these two high mountain systems during this time period. Genetic data sets supporting these biogeographical links The postglacial disjunction has not been sufficiently long for animals are (to my knowledge) not available at the for the evolution of a clear differentiation between these moment, but genetic data on plants support these connec- now disjunct parts of the distribution. Similar patterns are tions e.g. in the species Pulsatilla vernalis [65] and Polygo- also known for mountain plant species [47,62-66]. In the natum verticillatum [38]. Considering morphological case of Carex curvula, the Pyrenean populations are nested studies, the western Balkan populations of Erebia pandrose within the western Alps group and show a low level of in the high mountain systems of Monte Negro, Serbia and genetic diversity, probably due to recent long distance col- Macedonia are closely related with populations existing in onisation [67].

Links between northeastern Alps and northwestern Carpathians As in the case of the Pyrenees-Alps connections, many bio- geographical interactions exist between the northeastern Alps and the northwestern Carpathians (i.e. Tatra Mts.). Typical examples are found in distribution patterns of lep- idopterans like Pieris bryoniae and [49]. An mtDNA analysis of the wolf spider species complex Par- dosa saltuaria also underlines this link as the same mtDNA lineage was detected in the Alps and Carpathians (Figure 3) [43].

So far other genetic data for animals are lacking, but data on plants support this biogeographical link (e.g. for Prit- zelago alpina [36] and Senecio carniolicus [48]). For Ranun- culus alpestris, the Carpathians have been colonised EuropeanFigureGeographicallozyme 5 polymorphism mountain distribution systemss of of four the butterflygenetic lineages Erebia euryalebased onin the stepwise from an eastern Alpine lineage [68], and the arc- Geographic distribution of four genetic lineages tic-alpine Ranunculus pygmaeus colonised the Alps rela- based on allozyme polymorphisms of the butterfly tively recently from the east through the Tatra Mts. [69]. A Erebia euryale in the European mountain systems. Each lineage is presented in a different colour; separate areas relatively similar genetic link was observed between the marked by identical colour harbour the same lineage and are northern Alps and the mountains of northern Moravia linked by a dotted line in the same colour. Redrawn from about 200 km west of the High Tatra Mts. for the butterfly Schmitt & Haubrich [51]. Erebia epiphron (Figure 4) [50].

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the southeastern Alps. This thus supports a recent (i.e. disjunctions as already postulated by Holdhaus in his Würm glacial) biogeographical link between these two landmark book in 1954 [5]. This proposal is largely sup- areas that are now separated by several hundreds of kilo- ported by many genetic analyses on plants [65,66,70,79- metres with no mountains over 2,000 m. On the contrary, 83] and animals (Figure 3) [42,43]. This argues for the the Erebia pandrose populations of the high mountain sys- wide distribution of these species in the periglacial tems Rila and Pirin in Bulgaria are strongly differentiated steppes between the northern glacier and the glaciated from this group, and more closely related with the popu- mountains in the South and postglacial retreat to higher lations from the southern Carpathians [71], thus under- altitudes in the South, and higher latitudes in the North. lining a biogeographical east-west split throughout the central Balkan Peninsula [72]. In butterflies, the mtDNA sequences of Erebia pandrose indicate a very close genetic connection between the pop- Links between southern Carpathians and eastern Balkan ulations from the Alps, Pyrenees and Scandinavia thus mountains supporting their recent (i.e. postglacial) disjunction. The Danube valley apparently has often acted as effective However, the individuals from the Rila in Bulgaria show a dispersal barrier between the Carpathians and the high stronger genetic differentiation from these other regions, mountain systems of the eastern Balkan Peninsula [20] thus supporting the idea that the Balkan populations were with Erebia medusa being a well studied case in the Lepi- not included in this large zonal distribution during the doptera [18]. However, many connections between the last glaciation, but survived in an area of southeastern mountain systems of these two areas are also known. Europe not linked to the main distribution [42]. A similar Thus, a morphometric study of the male genitalia of Erebia structure was also observed in the leaf beetle Nebria rufes- pandrose demonstrated high similarities between these cens, but the differences against the Balkan haplotypes two high mountain areas [71] and hereby also supported were even stronger in this case [42]. Another butterfly a close biogeographical link between them. study with the lycaenid Aricia artaxerxes revealed a very weak genetic differentiation between the populations An allozyme analysis of the mountain forest species Erebia from the northern UK and Scandinavia of only one or two euryale revealed by far the highest genetic diversity in this mutations in the mtDNA cytochrome-b gene thus sup- species in the populations from the Bulgarian Rila and the porting the idea of a common source and only postglacial Romanian southern Carpathians, but no significant dif- isolation [84]. A rather similar genetic structure was ferentiation was detectable between these two areas (Fig- observed for the diving beetle Hydroporus glabriusculus ure 5) [51]. This is most probably due to the fact that these [85]. The mountain hare Lepus timidus showed genetically two areas were linked by cool forested areas during at least very similar populations in the Alps and in Fennoscandia the last ice age allowing massive gene flow between these analysed by allozymes [86] microsatellites and mtDNA two regions; thus, at least the region of the Iron Gate (pas- [87] underlining a postglacial common source for both sage of the Danube through the southern Carpathians) regions between the Alpine and the Fennoscandian ice- must have been extensively covered by this type of forest shields. The lack of genetic differentiation between the during this time period. Furthermore, this study supports Alps and Pyrenees in the arctic-alpine burnet Zygaena exu- the conclusion of other analyses based on fossil remains lans also supports the idea of a survival of this species in a (e.g. pollen, remains of animals) [73-78] that southeast- large zonal distribution range in the periglacial area of ern Europe was the most important glacial retreat of the Europe during the last ice age and postglacial retraction to representatives of the European mountain forest biome. the high mountain systems and the Arctic [88].

Furthermore, the distribution of many mountain species Genetic connections of middle high mountain (e.g. Erebia melas, E. cassioides, Coenonympha rhodopensis) systems in the Bulgarian high mountain systems and the southern The middle high mountain systems of Europe show Carpathians underlines the biogeographical connections numerous biogeographical connections with the high of the high mountain biota of both areas [20]. Genetic mountain systems and among each other. Thus, the links between both areas are also known for plant species French Massif Central shows strong connections with the [67]. Pyrenees in many cases, e.g. by having the same melanistic subspecies Erebia manto constans [49] as well as showing Genetic links between high mountain systems rather weak genetic differentiation in Parnassius apollo [89] and the Arctic and Pulsatilla vernalis [65]. However, in other cases, close Recent (i.e. late glacial or postglacial) genetic links connections exist between the Massif Central and the between the high mountain systems in the South and the Alps, as in the plant Polygonatum verticillatum [38]. How- Arctic in the North are a rather common biogeographical ever, the populations of the Massif Central are detected as characteristic of many species with typical arctic-alpine

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even an independent phylogeographic group, as in the case of the caddisfly Drusus discolor (Figure 2) [41].

Links with the Alps are known for the Bavarian and Bohe- mian Forest, e.g. by sharing the eastern Alpine lineage in the caddisfly Drusus discolor (Figure 2) [41], and for the Jesenik mountains in northern Moravia, e.g. by striking genetic similarities with northern Alps E. epiphron popula- tions (Figure 4) [50]. Relicts of alpine species in the Vos- ges and (to a lesser degree) in the Black Forest (e.g. in butterflies Erebia epiphron, E. manto, Clossiana titania, C. thore) [49] underline their close biogeographical relation with the Alps, which is also supported by genetic studies e.g. in the plant Polygonatum verticillatum [38]. In Pulsatilla vernalis, Tatra and Sudeten Mts. share the same chloro- plast haplotype indicating a close link between these two mountain ranges for this species, but isolation from the GeographicmetricstanicaFigure in 6ofthe the distributionEuropean male geni mountain taliaof three of the systemslineages caddisfly based Rhyacophila on morpho- aqui- Alps [65]. These patterns are most likely due to glacial ref- Geographic distribution of three lineages based on uge areas in the vicinity of the Alps, Carpathians or Pyr- morphometrics of the male genitalia of the caddisfly enees and postglacial retreat into one of these high Rhyacophila aquitanica in the European mountain mountain systems, but also into at least one of the adjoin- systems. Each lineage is presented in a different colour; sep- arate areas marked by identical colour harbour the same lin- ing middle high mountain systems with not sufficient eage. Redrawn from Bálint et al. [90]. time for differentiation since then.

Close biogeographical connections were also revealed among these middle high mountain systems. One striking postglacial into both of them is commonly resulting in example is the caddisfly Drusus discolor showing the same one genetic lineage being found in two different moun- mtDNA lineage in the COI gene in middle high mountain tain systems. systems (Figure 2) [41]. A similar pattern was also obtained in a morphometric study of another caddisfly Competing interests species Rhyacophila aquitanica with very similar popula- The author declares that he has no competing interests. tions in the French Massif Central, the Vosges, the Black Forest and the Swiss canton of Fribourg (Figure 6) [90]. References These patterns most probably result from a glacial distri- 1. Hewitt GM: Some genetic consequences of ice ages, and their role in divergence and speciation. Biol J Linn Soc 1996, bution in the lower altitudes between these middle high 58:247-276. mountain areas and postglacial retreat into the higher alti- 2. Schmitt T: Molecular biogeography of Europe: Pleistocene tudes of these adjoining mountains. cycles and postglacial trends. Front Zool 2007, 4:11. 3. Taberlet P, Fumagalli L, Wust-Saucy A-G, Cosson J-F: Comparative phylogeography and postglacial colonization routes in Conclusion Europe. Mol Ecol 1998, 7:453-464. The topology of the European mountain systems had a 4. Hewitt GM: Post-glacial re-colonization of European biota. Biol J Linn Soc 1999, 68:87-112. strong influence on the biogeography and evolution of 5. Holdhaus K: Die Spuren der Eiszeit in der Tierwelt Europas. mountain and high latitude species. Due to the dynamic Abh zool-bot Ges Wien 1954, 18:1-493. 6. de Lattin G: Grundriss der Zoogeographie. Stuttgart, Fischer; changes of these biota over time, a large variety of differ- 1967. ent evolutionary processes are responsible for the devel- 7. Reinig W: Die Holarktis. Jena, Fischer; 1937. opment of numerous biogeographical patterns. The most 8. de Lattin G: Beiträge zur Zoogeographie des Mittelmeergebi- etes. Verh deut Zool Ges, Kiel 1949:143-151. simple of these is the evolution of one genetic lineage or 9. Hewitt GM: The genetic legacy of the Quaternary ice ages. species endemic to one single mountain system due to Nature 2000, 405:907-913. 10. Habel JC, Schmitt T, Müller P: The fourth paradigm pattern of vicariance with subsequent long processes of geographic postglacial range expansion of European terrestrial species: isolation and evolution, as observed in almost all Euro- the phylogeography of the Marbled White butterfly (Satyri- pean high mountain systems. Especially in the Alps, but nae, ). J Biogeogr 2005, 32:1489-1497. 11. Schmitt T, Seitz A: Intraspecific allozymatic differentiation also in smaller high mountain systems, different genetic reveals the glacial refugia and the postglacial expansions of lineages exist beside each other as a result of evolution in European Erebia medusa (Lepidoptera: ). Biol J geographically isolated areas, with often secondary con- Linn Soc 2001, 74:429-458. 12. Babik W, Branicki W, Sandera M, Litvinchuk S, Borkin LJ, Irwin JT, tacts in these mountain systems. Where such centres of Rafinki J: Mitochondrial phylogeography of the moor frog, evolution and differentiation of lineages were located Rana arvalis. Mol Ecol 2004, 13:1469-1480. 13. Pinceel J, Jordaens K, Pfenninger M, Backeljau T: Rangewide phylo- between two mountain systems, retraction during the geography of a terrestrial slug in Europe: evidence for Alpine

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